Molecular basis and ecological genetics of hybrid incompatibilities involving a balanced NPR1 polymorphism in the genus Capsella

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The establishment of gene-flow barriers during speciation is described by the Bateson-Dobzhansky-Muller model of hybrid incompatibilities. According to this model, novel alleles that become fixed in separated populations interact negatively in hybrids and decrease their fitness. In plants, many such incompatibilities are polymorphic, with compatible and incompatible alleles present in the species or populations. This suggests an important role of genetic drift and/or balancing selection in the formation of hybrid incompatibilities. We have recently characterized the molecular basis of a polymorphic incompatibility between the incipient species Capsella grandiflora and C. rubella involving the two pathogen-response genes NPR1 and RPP5. While the incompatible RPP5 allele appears to have arisen by a novel mutation in C. rubella, both compatible and incompatible NPR1 alleles are present at high frequencies in C. grandiflora; by contrast, C. rubella is fixed for the compatible NPR1 allele. The two NPR1 alleles have been maintained by balancing selection in C. grandiflora, possibly reflecting their functional specialization in setting the basal level of pathogen response. From further crosses between different C. grandiflora and C. rubella accessions, we have identified three more hybrid incompatibilities involving NPR1 and at least one other locus distinct from RPP5. These findings suggest that the long-term maintenance of functionally divergent alleles by balancing selection and their divergent lineage sorting facilitate the establishment of Bateson-Dobzhansky-Muller incompatibilities between incipient species. This project will investigate the molecular basis and ecological genetics of hybrid incompatibilities involving the balanced NPR1 polymorphism by focussing on three objectives. (1) We will determine the causal mutation in the incompatible RPP5 allele and study its effect on the interaction between RPP5 and NPR1, as well as its evolutionary history. (2) We will identify the other incompatible loci for the additional NPR1-dependent incompatibilities between C. grandiflora and C. rubella, determine the causal mutations and study their evolutionary history and population genetics. (3) The basis of the observed balancing selection on NPR1 in C. grandiflora will be investigated by characterizing the leaf- and root-associated microbiome of individuals sampled in their natural habitat in Central Greece; microbiome-parameters will be associated with the NPR1 genotype of the plants to test different hypotheses about the balancing selection on NPR1. Any associations will be followed up by plant growth experiments using defined microbiome compositions. Together, these studies will provide important novel insight into the evolutionary and ecological genetics of hybrid incompatibilities in Capsella that are likely to be relevant more broadly to plant speciation associated with the outbreeding-to-selfing transition.